The Role of the Amygdala and Orbital frontal Cortex in Processing Socially Relevant Crossmodal Signals Open Access

Payne, Christa (2011)

Permanent URL: https://etd.library.emory.edu/concern/etds/4j03cz84c?locale=en
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Abstract

Abstract
The Role of the Amygdala and Orbital Frontal Cortex in Processing
Socially Relevant Crossmodal Signals
Primate social success requires crossmodal integration of affective social signals
from faces and voices, but little is known about the neural substrates supporting
this ability. Hence, we assessed the contributions of amygdala and orbital frontal
cortex in the acquisition of normal integration and affective processing abilities. Integration
ability and scanning strategies of 16 adult rhesus macaques that received either
lesions of the amygdala (Neo-Aibo; n = 6) or the orbital frontal cortex (Neo-Oasp; n
= 4) or sham operations (Ne0-C; n = 6) as infants (males = females in each
group) were quantified using eye-tracking. Four short (2-sec) video clips
depicting novel male conspecifics producing one of four species-typical
vocalizations (coo, grunt, scream, threat) were presented in a preferential viewing
paradigm. Pairs of videos were played with the auditory component matching one
of vocalizations in two conditions: Synchronized (simultaneous onset of audio
and visual components); Desynchronized (delayed onset of audio component).
Group Neo-C showed a preference for one of the two videos in both conditions,
indicating integration ability. Scanning patterns of males and females differed,
with females (eyes > mouth) attending to vocalization valence, but males (eyes =
mouth) appeared to also attend to another stimulus feature, such as the inferred
dominance status of the stimulus animals. Group Neo-Aibo demonstrated normal
integration ability, but the sex-specific scanning strategies exhibited by group
Neo-C were completely disrupted. Neo-Aibo males and females showed the exact
opposite pattern of group Neo-C. By contrast, group Neo-Oasp showed weakened
integration ability that was associated with increased looking to the eye regions.
This increased salience of the eyes was attributed to higher aggression displayed
by these monkeys in other laboratory measures. Collectively, our data show that
both the amygdala and orbital frontal cortex are involved in the evaluation of
socio-emotional audiovisual signals, albeit in slightly different ways. In line with
current literature, the amygdala appears to contribute to sex-specific assessments
of the social salience of the crossmodal stimuli, whereas the orbital frontal cortex
is crucial for the appropriate regulation of responses to the stimuli.

Table of Contents

Table of Contents

GENERAL INTRODUCTION 1

1- Terminology___________________________________________________________ 3

2- Dynamic vs. Static Stimuli________________________________________________ 7

3- Rhesus Macaque Vocalizations_____________________________________________ 8

4- Amygdala and Socio-emotional Processing___________________________________ 10

A) Sensory Convergence in the Amygdala______________________________________ 13

B) Amygdala and Emotion__________________________________________________ 14

i) Amygdala and Facial Emotion______________________________________________ 15

ii) Amygdala and Vocal Emotion______________________________________________ 16

iii) Amygdala and Audiovisual Emotion_________________________________________ 17

5- Orbital Frontal Cortex and Socio-emotional Processing__________________________ 21

A) Sensory Convergence in the Orbital Frontal Cortex_____________________________ 21

B) Orbital Frontal Cortex and Emotion_________________________________________ 22

i) Orbital Frontal Cortex and Facial Emotion_____________________________________ 23

ii) Orbital Frontal Cortex and Auditory Emotion__________________________________ 24

iii) Orbital Frontal Cortex and Audiovisual Emotion_______________________________ 25

6- Specific Aims and Hypotheses_____________________________________________ 27

MANUSCRIPT I: Crossmodal Integration of Conspecific Vocalizations in Rhesus Macaques 31

Abstract________________________________________________________________ 32

Introduction_____________________________________________________________ 34

Method_________________________________________________________________ 36

Subjects________________________________________________________________ 37

Crossmodal integration task________________________________________________ 37

Measures_______________________________________________________________ 39

Statistical Analyses_______________________________________________________ 40

Results_________________________________________________________________ 41

Overall Integration and Scanning Patterns_____________________________________ 41

Identity________________________________________________________________ 44

Valence________________________________________________________________ 47

Discussion______________________________________________________________ 51

Viewing of eye regions____________________________________________________ 51

Sex differences in scanning patterns_________________________________________ 53

Additional influences on looking behavior_____________________________________ 56

Conclusions____________________________________________________________ 58

Acknowledgements______________________________________________________ 60

Figures________________________________________________________________ 61

MS-I Figure 1: Schematic of Stimulus Presentation with ROIs._____________________ 62

MS-I Figure 2: Integration Assessment - All Trials.______________________________ 63

MS-I Figure 3: Scanning Patterns - All Trials.___________________________________ 64

MS-I Figure 4: Sex Differences - All Trials._____________________________________ 65

MS-I Figure 5: Integration Assessment - Relative Identity._________________________ 66

MS-I Figure 6: Scanning Patterns - Identity Trials._______________________________ 67

MS-I Figure 7: Sex Differences - Identity Different Trials.__________________________ 68

MS-I Figure 8: Integration Assessment - Relative Valence._________________________ 69

MS-I Figure 9: Scanning Pattern - Valence Trials._________________________________ 70

MS-I Figure 10: Sex Differences - Valence Same Trials.____________________________ 71

MS-I Figure 11: Relative Looking to Eyes and Mouths by Males and Females.___________ 72

MS-I Figure 11: Representative Scan Paths for Males and Females.___________________ 73

References_______________________________________________________________ 74

MANUSCRIPT II: The Role of the Amygdala in Processing Bimodal Conspecific Vocalizations in Rhesus Macaques 83

Abstract_________________________________________________________________ 84

Introduction______________________________________________________________ 86

Method__________________________________________________________________ 89

Subjects_________________________________________________________________ 89

Magnetic Resonance Imaging Procedures_______________________________________ 90

Determination of Neonatal Amygdala Injection Coordinates_________________________ 91

Surgical Procedures________________________________________________________ 92

Lesion Verification_________________________________________________________ 93

Crossmodal integration task_________________________________________________ 94

Measures_______________________________________________________________ 96

Statistical Analyses________________________________________________________ 97

Results_________________________________________________________________ 98

Overall Integration and Scanning Patterns______________________________________ 98

Identity_________________________________________________________________ 101

Valence_________________________________________________________________ 105

Discussion_______________________________________________________________ 109

Retained Integration Ability__________________________________________________ 110

Disruption of scanning strategies_____________________________________________ 112

Disruption of species-specific responses________________________________________ 113

Additional influences on looking behavior_______________________________________ 115

Conclusions______________________________________________________________ 117

Acknowledgements________________________________________________________ 117

Tables & Figures.__________________________________________________________ 119

MS-II Table 1: Extent of Lesion Assessment._____________________________________ 120

MS-II Figure 1. Intended lesion and representative case for Neo-Aibo._________________ 121

MS-II Figure 2: Schematic of Stimulus Presentation with ROIs.______________________ 122

MS-II Figure 3: Integration Assessment - All Trials._______________________________ 123

MS-II Figure 4: Scanning Patterns - All Trials.____________________________________ 124

MS-II Figure 5: Sex Differences - All Trials.______________________________________ 125

MS-II Figure 6: Integration Assessment - Relative Identity._________________________ 126

MS-II Figure 7: Scanning Patterns - Identity Trials.________________________________ 127

MS-II Figure 8: Sex Differences - Identity Different Trials.___________________________ 128

MS-II Figure 9: Integration Assessment - Relative Valence.__________________________ 129

MS-II Figure 10: Scanning Pattern - Valence Trials.________________________________ 130

MS-II Figure 11: Sex Differences - Valence Same Trials.____________________________ 131

MS-II Figure 12: Representative Scan Paths - Males._______________________________ 132

MS-II Figure 13: Representative Scan Paths - Females._____________________________ 133

References________________________________________________________________ 134

MANUSCRIPT III: The Role of the Orbital Frontal Cortex in Processing Bimodal Conspecific Vocalizations in Rhesus Macaques 143

Abstract__________________________________________________________________ 144

Introduction_______________________________________________________________ 146

Method___________________________________________________________________ 148

Subjects__________________________________________________________________ 148

Magnetic Resonance Imaging Procedures________________________________________ 149

Surgical Procedures_________________________________________________________ 150

Lesion Verification__________________________________________________________ 151

Crossmodal integration task__________________________________________________ 152

Measures_________________________________________________________________ 154

Statistical Analyses_________________________________________________________ 155

Results__________________________________________________________________ 156

Integration Assessment after Neonatal Orbital Frontal Lesions_______________________ 156

Scanning Patterns after Neonatal Orbital Frontal Lesion____________________________ 161

Discussion_______________________________________________________________ 167

Weaker ability to integrate bimodal social signals_________________________________ 167

Inflexibility of Scanning Strategies_____________________________________________ 169

Increased Aggression_______________________________________________________ 172

Conclusions_______________________________________________________________ 175

Acknowledgements_________________________________________________________ 176

Tables & Figures.___________________________________________________________ 177

MSIII - Table 1: Extent of Lesion Assessment.____________________________________ 178

MSIII - Figure 1. Intended lesion and representative case.__________________________ 179

MSIII - Figure 2: Schematic of Stimulus Presentation with ROIs.______________________ 180

MSIII - Figure 3: Integration Assessment - All Trials._______________________________ 181

MSIII - Figure 4: Integration Assessment - Relative Identity._________________________ 182

MSIII - Figure 5: Integration Assessment - Relative Valence._________________________ 183

MSIII - Figure 6: Scanning Patterns - All Trials.____________________________________ 184

MSIII - Figure 7: Scanning Patterns - Identity Trials.________________________________ 185

MSIII - Figure 8: Sex Differences - Identity Different Trials.__________________________ 186

MSIII - Figure 9: Scanning Patterns - Valence Trials.________________________________ 187

MSIII - Figure 10: Sex Differences - Valence Same Trials.____________________________ 188

MSIII - Figure 11: Representative Scan Paths - Males._______________________________ 189

MSIII - Figure 12: Representative Scan Paths - Females._____________________________ 190

References__________________________________________________________________ 191

GENERAL DISCUSSION 200

1- How do rhesus macaques integrate crossmodal social signals?_______________________ 201

A) Integration and scanning patterns_____________________________________________ 201

B) Species-specific scanning patterns_____________________________________________ 203

2- Effects of neonatal amygdala and orbital frontal cortex_____________________________ 205

A) Amygdala lesions__________________________________________________________ 205

B) Effects of orbital frontal lesions_______________________________________________ 206

C) Comparisons of the neonatal amygdala and orbital frontal lesions.___________________ 207

3- Neural network of Emotional Crossmodal Integration______________________________ 210

A) Fusiform Gyrus___________________________________________________________ 210

B) Middle and Superior Temporal Areas___________________________________________ 211

C) Amygdala________________________________________________________________ 213

D) Orbital Frontal Cortex______________________________________________________ 214

E) Summary________________________________________________________________ 216

4- Does the Amygdala Modulate Evaluations of Socio-emotional Audiovisual Information?________________________________________________________________ 216

A) Amygdala and integration of crossmodal social cues_______________________________ 216

B) Amygdala and scanning patterns of faces_______________________________________ 217

C) Amygdala and sex differences________________________________________________ 219

5- Does the Orbital Frontal Cortex Modulate Emotional Audiovisual Integration?________________________________________________________________ 220

A) Orbital frontal cortex and integration of crossmodal social cues______________________ 221

B) Orbital frontal cortex and scanning patterns of faces______________________________ 221

6- Do the Amygdala and Orbital Frontal Cortex Uniquely Contribute to Emotional Crossmodal Integration?_______________________________________________________________ 224

7- Translation to Human Neuropsychopathology___________________________________ 225

8- Concluding Remarks______________________________________________________ 228

General Discussion - Tables & Figures.___________________________________________ 230

Table 1: Summary of Crossmodal Integration Abilities and Scanning Patterns.__________________________________________________________________ 231

Figure D1: Group Summary of Integration Assessments - All Trials.____________________ 232

Figure D2: Group Summary of Integration Assessments.____________________________ 233

Figure D3: Group Summary of Scanning Patterns - All Trials._________________________ 234

Figure D4: Group Summary of Scanning Patterns - Identity and Valence._______________ 235

Figure D5: Group Summary of Sex Differences - All Trials.___________________________ 236

Figure D6: Group Summary of Sex Differences - Identity and Valence._________________ 237

Figure D7: Representation of Neural Network Subserving Emotional Crossmodal Integration. 238

GENERAL REFERENCES 239

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